Abstract
Despite the agricultural importance of both potato and tomato, very little is known about their chloroplast genomes. Analysis of the complete sequences of tomato, potato, tobacco, and Atropa chloroplast genomes reveals significant insertions and deletions within certain coding regions or regulatory sequences (e.g., deletion of repeated sequences within 16S rRNA, ycf2 or ribosomal binding sites in ycf2). RNA, photosynthesis, and atp synthase genes are the least divergent and the most divergent genes are clpP, cemA, ccsA, and matK. Repeat analyses identified 33–45 direct and inverted repeats ≥30 bp with a sequence identity of at least 90%; all but five of the repeats shared by all four Solanaceae genomes are located in the same genes or intergenic regions, suggesting a functional role. A comprehensive genome-wide analysis of all coding sequences and intergenic spacer regions was done for the first time in chloroplast genomes. Only four spacer regions are fully conserved (100% sequence identity) among all genomes; deletions or insertions within some intergenic spacer regions result in less than 25% sequence identity, underscoring the importance of choosing appropriate intergenic spacers for plastid transformation and providing valuable new information for phylogenetic utility of the chloroplast intergenic spacer regions. Comparison of coding sequences with expressed sequence tags showed considerable amount of variation, resulting in amino acid changes; none of the C-to-U conversions observed in potato and tomato were conserved in tobacco and Atropa. It is possible that there has been a loss of conserved editing sites in potato and tomato.
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Asano T, Tsudzuki T, Takahashi S, Shimada H, Kadowaki K (2004) Complete nucleotide sequence of the sugarcane (Saccharum officinarum) chloroplast genome: a comparative analysis of four monocot chloroplast genomes. DNA Res 11:93–99
Bausher MG, Singh ND, Mozoru J, Lee S-B, Jansen RK, Daniell H (2006) The complete chloroplast genome sequence of Citrus sinensis (L.) Osbeck var. ‘Ridge Pineapple’: organization and phylogenetic relationships to other angiosperms. BMC Plant Biol (in review)
Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103
Bohs L, Olmstead RG (1997) Phylogenetic relationships in Solanum (Solanaceae) based on ndhF sequences. Syst Bot 22:5–17
Bowman CM, Dyer T (1986) The location and possible evolutionary significance of small dispersed repeats in wheat ctDNA. Curr Genet 10:931–941
Cosner ME, Jansen RK, Palmer JD, Downie SR (1997) The highly rearranged chloroplast genome of Trachelium caeruleum (Campanulaceae): Multiple inversions, inverted repeat expansion and contraction, transposition, insertions/deletions, and several repeat families. Curr Genet 31:419–429
Cui L, Veeraraghavan N, Wall K, Jansen RK, Leebens-Mack J, Makalowska I, dePamphilis CW (2006) ChloroplastDB: the chloroplast genome database. Nucleic Acids Res 34:D692–D696
Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20:581–586
Daniell H, Datta R, Varma S, Gray S, Lee S-B (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat Biotechnol 16:345–348
Daniell H, Lee S-B, Panchal T, Wiebe PO (2001) Expression of cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. J Mol Biol 311:1001–1009
Daniell H, Khan M, Allison L (2002) Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. Trends Plant Sci 7:84–91
Daniell H, Carmona-Sanchez O, Burns BB (2004a) Chloroplast-derived vaccine antibodies, biopharmaceuticals, and edible vaccines in transgenic plants engineered via the chloroplast genome. In: Schillberg S (ed) Molecular farming. Wiley, Germany, Chapter 8 pp 113–133
Daniell H, Cohill PR, Kumar S, Dufourmantel N (2004b) Chloroplast genetic engineering In: Daniell H, Chase CD (eds) molecular biology and biotechnology of plant organelles. Springer Publishers, Netherlands, pp 443–490
Daniell H, Kumar S, Duformantel N (2005) Breakthrough in chloroplast genetic engineering of agronomically important crops. Trends Biotechnol 23(5):238–245
DeCosa B, Moar W, Lee S-B, Miller M, Daniell H (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 9:71–74
DeGray G, Rajasekaran K, Smith F, Sanford J, Daniell H (2001) Expression of an antimicrobial peptide via the chloroplast genome to control phytopathogenic bacteria and fungi. Plant Physiol 127:852–862
Dhingra A, Portis AR, Daniell H (2004) Enhanced translation of a chloroplast expressed rbcS gene restores SSU levels and photosynthesis in nuclear antisense RbcS plants. Proc Natl Acad Sci USA 101:6315–6320
Dufourmantel N, Pelissier B, Garçon F, Peltier JM, Tissot G (2004) Generation of fertile transplastomic soybean. Plant Mol Biol 55(4):479–89
Elnitski L, Riemer C, Petrykowska H et al (2002) PipTools: a computational toolkit to annotate and analyze pairwise comparisons of genomic sequences. Genomics 80:681–690
Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred II error probabilities. Genome Res 8:186–194
Fernandez-San Millan A, Mingo-Castel A, Miller M, Daniell H (2003) A chloroplast transgenic approach to hyper express and purify human serum albumin, a protein highly susceptible to proteolytic degradation. Plant Biotechnol J 1:71–79
Fiebig A, Stegemann S, Bock R (2004) Rapid evolution of RNA editing sites in a small non-essential plastid gene. Nucleic Acids Res 32:3615–3622
Goulding SE, Olmstead RG, Morden CW, Wolfe KH (1996) Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet 252:195–206
Grevich JJ, Daniell H (2005) Chloroplast genetic engineering: Recent advances and future perspectives. Crit Rev Plant Sci 24:83–108
Guda C, Lee S-B, Daniell H (2000) Stable expression of biodegradable protein based polymer in tobacco chloroplasts. Plant Cell Rep 19:257–262
Hagemann R (2004) The sexual inheritance of plant organelles. In: Daniell H, Chase C (eds) Molecular biology and biotechnology of plant organelles. Springer Publishers, Dordrecht, pp 93–113
Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Meth Enzymol 266:383–402
Hiratsuka J, Shimada H, Whittier R et al (1989) The complete sequence of rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194
Hirose T, Kusumegi T, Tsudzuki T, Sugiura M (1999) RNA editing sites in tobacco chloroplast transcripts: editing as a possible regulator of chloroplast RNA polymerase activity. Mol Gen Genet 262:462–467
Howe CJ (1985) The endpoints of an inversion in wheat chloroplast DNA are associated with short repeated sequences containing homology to att-lambda. Curr Genet 10:139–145
Hupfer H, Swaitek M, Hornung S et al. (2000) Complete nucleotide sequence of the Oenothera elata plastid chromosome, representing plastome 1 of the five distinguishable Euoenthera plastomes. Mol Gen Genet 263:581–585
Iamtham S, Day A (2000) Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat Biotechnol 18:1172–1176
Jansen RK, Raubeson LA, Boore JL et al (2005) Methods for obtaining and analyzing chloroplast genome sequences. Meth Enzym 395:348–384
Jansen RK, Kaittanis C, Saski C, Lee S-B, Tompkins J, Alverson AJ, Daniell H (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol (in press)
Kato T, Kaneko T, Sato S, Nakamura Y, Tabata S (2000) Complete structure of the chloroplast genome of a legume, Lotus japonicus. DNA Res 7:323–330
Kelchner SA (2002) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Missouri Bot Gard 87:482–498
Kim K-J, Lee H-L (2004) Complete chloroplast genome sequence from Korean Ginseng (Panax schiseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res 11:247–261
Kim J-S, Jung JD, Lee J-A et al. (2006) Complete sequence and organization of the cucumber (Cucumis sativus L. cv. Baekmibaekdadagi) chloroplast genome. Plant Cell Rep, online
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Knox EB, Palmer JD (1998) Chloroplast DNA evidence on the origin and radiation of the giant lobelias in eastern Africa. Syst Bot 23:109–149
Kota M, Daniel H, Varma S, Garczynski SF, Gould F, William MJ (1999) Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc Natl Acad Sci USA 96:1840–1845
Koya V, Moayeri M, Leppla SH, Daniell H (2005) Plant based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infect Immun 73:8266–8274
Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423
Kumar S, Koichiro T, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245
Kumar S, Dhingra A, Daniell H (2004a) Plastid expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots and leaves confers enhanced salt tolerance. Plant Physiol 136:2843–2854
Kumar S, Dhingra A, Daniell H (2004b) Manipulation of gene expression facilitates plastid transformation of cotton by somatic embryogenesis and maternal inheritance of transgenes. Plant Mol Biol 56:203–216
Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642
Lee S-B, Kwon H-B, Kwon S-J et al. (2003) Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11:1–13
Lee S-B, Kaittanis C, Hostetler J, Town C, Jansen RK, Daniell H (2006) The complete chloroplast genome sequence of Gossypium hirsutum: organization and phylogenetic relationships to other angiosperms. BMC Genomics (in press)
Leelavathi S, Reddy VS (2003) Chloroplast expression of His-tagged GUS-fusions: a general strategy to overproduce and purify foreign proteins using transplastomic plants as bioreactors. Mol Breed 11:49–58
Leelavathi S, Gupta N, Maiti S, Ghosh A, Reddy VS (2003) Overproduction of an alkali-and thermo-stable xylanase in tobacco chloroplasts and efficient recovery of the enzyme. Mol Breed 11:59–67
Lossl A, Eibl C, Harloff HJ, Jung C, Koop HU (2003) Polyester synthesis in transplastomic tobacco (Nicotiana tabacum L): significant contents of polyhydroxybutyrate are associated with growth reduction. Plant Cell Rep 21:891–899
Maier RM, Schmitz-Linneweber (2004) Plastid genomes. In: Daniell H Chase CD (eds) Molecular biology and biotechnology of plant organelles. Springer publishers, Netherlands, pp 115–150
Maier RM, Neckermann K, lgloi GL, Kossel H (1995) Complete sequence of the maize chloroplast genome: Gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol 251:614–628
Masood MS, Nishikawa T, Fukuoka S, Njenga PK, Tsudzuki T, Kadowaki K (2004) The complete nucleotide sequence of wild rice (Oryza nivara) chloroplast genome: first genome wide comparative sequence analysis of wild and cultivated rice. Gene 340:133–139
Matsuoka Y, Yamazaki Y, Ogihara Y, Tsunewaki K (2002) Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals. Mol Biol Evol 19:2084–2091
Maul JE, Lilly JW, Cui L et al. (2002) The Chlamydomonas reinhardtii plastid chromosome: Islands of genes in a sea of repeats. The plant Cell 14:1–22
McBride KE, Svab Z, Schaaf DJ, Hogan PS, Stalker DM, Maliga P (1995) Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Bio Technol 13:362–365
Milligan BG, Hampton JN, Palmer JD (1989) Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol Biol Evol 6:355–368
Molina A, Herva-Stubbs S, Daniell H, Mingo-Castel AM, Veramendi J (2004) High yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant Biotechnol J 2:141–153
Nguyen TT, Nugent G, Cardi T, Dix PJ (2005) Generation of homoplasmic plastid transformants of a commercial cultivar of potato (Solanum tuberosum L). Plant Sci 168:1495–1500
Ogihara Y, Isono K, Kojima T et al. (2000) Chinese spring wheat (Triticum aestivum L.) chloroplast genome: complete sequence and contig clones. Plant Mol Biol Rep 18:243–253
Olmstead RG, Sweere JA, Spangler RE, Bohs L, Palmer JD (1999) Phylogeny and provisional classification of the Solanaceae based on chloroplast DNA. In: Nee M, Symon DE, Jessup JP, Hawkes JG (eds) Solanaceae IV, advances in biology and utilization. Royal Botanic Gardens, Kew, pp 111–137
Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Hermann RG (ed) The molecular biology of plastids. Cell culture and somatic cell genetics of plants, vol 7A. Springer-Verlag, Vienna, pp 5–53
Palmer JD, Nugent JM, Herbon LA (1987) Unusual structure of Geranium chloroplast DNA—a triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families. Proc Natl Acad Sci USA 84:769–773
Palmer JD, Osorio B, Thompson WF (1988) Evolutionary significance of inversions in Legume chloroplast DNAs. Curr Genet 14:65–74
Quesada-Vargas T, Ruiz ON, Daniell H (2005) Characterization of heterologous multigene operons in transgenic chloroplasts: transcription, processing, translation. Plant Physiol 138:1746–1762
Raubeson LA, Jansen RK (2005) Chloroplast genomes of plants. In: Henry R (ed) Diversity and evolution of plants-genotypic and phenotypic variation in higher plants. CABI Publishing, Wallingford, pp 45–68
Ruf S, Hermann M, Berger I, Carrer H, Bock R (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat Biotechnol 19:870–875
Ruiz ON, Daniell H (2005) Engineering. cytoplasmic male sterility via the chloroplast genome. Plant Phys 138:1232–1246
Ruiz ON, Hussein H, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Phys 32:1344–1352
Saski C, Lee S-B, Daniell HT et al. (2005) Complete chloroplast genome sequence of Glycine max and comparative analyses with other legume genomes. Plant Mol Biol 59:309–322
Schmitz-Linneweber C, Maier RM, Alcaraz JP, Cottet A, Herrmann RG, Mache R (2001) The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization. Plant Mol Biol 45:307–315
Schmitz-Linneweber C, Regel R, Du TG, Hupfer H, Herrmann RG, Maier RM (2002) The plastid chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: the role of RNA editing in generating divergence in the process of plant speciation. Mol Biol Evol 19:1602–1612
Schwartz S, Elnitski L, Li M et al. (2003) MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res 31:3518–3524
Scott SE, Wilkenson MJ (1999) Low probability of chloroplast movement from oilseed rape (Brassica napus) into wild Brassica rapa. Nat Biotechnol 17:390–392
Sears BB, Stoike LL, Chiu WL (1996) Proliferation of direct repeats near the Oenothera chloroplast DNA origin of replication. Mol Biol Evol 13:850–863
Shaw J, Lickey EB, Beck JT et al. (2005) The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analyses. Am J Bot 92:142–166
Shinozaki K, Ohme M, Tanaka et al. (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. The EMBO J 5:2043–2049
Sidorov VA, Kasten D, Pang SZ, Hajdukiewicz PT, Staub JM, Nehra NS (1999) Technical advance: stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J 19:209–216
Spooner DM, Anderson GJ, Jansen RK (1993) Chloroplast DNA evidence for the interrelationships of Tomatoes, Potatoes, and Pepinos. Am J Bot 8:676–688
Staub JM, Garcia B, Graves J, Hajdukiewicz PTJ, Hunter P, Nehra N (2000) High-yield production of a human therapeutic protein in tobacco chloroplasts. Nat Biotechnol 18:333–338
Steane DA (2005) Complete nucleotide sequence of the chloroplast genome from the Tasmanian Blue Gum, Eucalyptus globules (Myrtaceae). DNA Res 12:215–220
Tang J, Xia H, Cao M (2004) A comparison of rice chloroplast genomes. Plant Phys 135:412–420
Tanksley SD, Ganal MW, Prince JP et al. (1992) High density molecular linkage maps of tomato and potato genomes. Genetics 132:1141–1160
Timme RE, Kuehl JV, Boore JL, Jansen RK (2006) A comparison of the first two sequenced chloroplast genomes in Asteraceae: Lettuce and Sunflower. BMC Evol Biol (in review)
Tregoning JS, Nixon P, Kuroda H et al. (2003) Expression of tetanus toxin Fragment C in tobacco chloroplasts. Nucleic Acids Res 31(4):1174–1179
Vitanen PV, Devine AL, Kahn S, Deuel DL, Van-Dyk DE, Daniell H (2004) Metabolic engineering of the chloroplast genome using the E coli ubiC gene reveals that corismate is a readily abundant precursor for 4-hydroxybenzoic acid synthesis in plants. Plant Phys 136:4048–4060
Vomstein J, Hachtel W (1988) Deletions, insertions, short inverted repeats, sequences resembling att-lambda, and frame shift mutated open reading frames are involved in chloroplast DNA differences in the genus Oenothera subsection Munzia. Mol Gen Genet 213:513–518
Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91:9794–9798
Watson J, Koya V, Leppla SH, Daniell H (2004) Expression of Bacillus anthracis protective antigen in transgenic chloroplasts of tobacco, a non-food/feed crop. Vaccine 22:4374–4384
Wolf PG, Rowe CA, Hasebe M (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339:89–97
Wyman SK, Boore JL, Jansen RK (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3255
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Investigations reported in this article were supported in part by grants from USDA 3611-21000-017-00D to Henry Daniell and from NSF DEB 0120709 to Robert K. Jansen.
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Daniell, H., Lee, SB., Grevich, J. et al. Complete chloroplast genome sequences of Solanum bulbocastanum, Solanum lycopersicum and comparative analyses with other Solanaceae genomes. Theor Appl Genet 112, 1503–1518 (2006). https://doi.org/10.1007/s00122-006-0254-x
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DOI: https://doi.org/10.1007/s00122-006-0254-x